Sci Parasitol 16(3):123-127, September 2015 ISSN 1582-1366 SHORT RESEARCH NOTE

Gastrointestinal helminths of the Caspian (Tetraogallus caspius) from the North ,

Amin Ahmadi1, Saeid Yaghfoori2, Vali Abedi3, Hassan Borji4

1 – MS.c, Ph.D Candidate of Veterinary Parasitology, Department of Pathobiology, School of Veterinary Medicine, Shiraz University, P.O. Box 1731, Shiraz 71345, Iran. 2 – MS.c, Ph.D Student of Veterinary Parasitology, Department of Pathobiology, School of Veterinary Medicine, Ferdowsi University of Mashhad, Iran. 3 – D.V.M, PhD. of Veterinary Parasitology, Office of Veterinary Medicine – North Khorasan. 4 – Associate professor of Veterinary Parasitology, Department of Pathobiology, School of Veterinary Medicine, Ferdowsi University of Mashhad, Iran. Correspondence: Tel. +98 9130363668, E-mail [email protected]

Abstract. The aim of this study was to establish the recognition of the parasitic infection of the (Tetraogallus caspius) partridge from the North Khorasan province that is one of the provinces located at the north east of Iran. In this study, 180 Caspian snowcock (Tetraogallus caspius) were randomly collected from different parts of North Khorasan region, during 2011-2012 to determine the presence and intensity of helminth infections in local Partridge of this geographic region. In the examination of alimentary tracts of these 180 partridges, it was found that 136 partridges were infected with parasitic helminths. At 132 cases were occurred infection with the cestode and 4 were infected with the nematodes.The number of partridges chickens infected with the both cestodes and nematodes were two. This study indicates the severity of the prevalence of gastrointestinal helminth infections in the indigenous Caspian snowcock of the North Khorasan province that has its own agro-climatic characteristics, and the country of Iran with highly diverse geographic and agro-climatic conditions.

Keywords: Partridge; Anonchotaenia globata; Raillietina tetragona; Ascaridia galli; Heterakis dispar; Trichostrongylus tenuis; Iran. Received 25/06/2015. Accepted 04/08/2015.

Introduction Mountains of the North of Iran. It is one of the five of snowcock in the The Caspian snowcock (Tetraogallus caspius) is Tetraogallus, part of the pheasant family a common species in , (). The population is thought to be , and throughout the Alborz declining, but not sufficiently rapidly to

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approach the thresholds used by Life and from different parts of North Khorasan region, IUCN as criteria for listing as threatened. Many during 2011-2012 to determine the presence problems are facing Caspian snowcock which and intensity of the helminthic infections in limit its activity, growth and vitality, including local partridges of this geographic region. competition, predation, parasites, diseases, hunting, accidents and habitat degradation. Under studied area: The North Khorasan Caspian snowcock issusceptible to many of the province is one of the provinces located at the common fowl parasites such as: protozoa, north east of Iran. The North Khorasan helminths, lice, fleas and mites (BirdLife, 2012). province is located in the mountainous area between 19,56°-43,57° longitude and 13,37°- The gastrointestinal parasites, especially the 17,38° latitude. This area, from north east to helminths, are the most common and the most north west is conterminous with lethal parasites affecting the indigenous , from west to south is limited to (Ashenafi and Eshetu, 2004; Mwale and Masika, the and from east 2011). It also has been observed that helminth and south-east to Golestanand Semnan infections that are present in rural free-range Provinces. chickens may result in subclinical diseases (Magwisha et al., 2002; Mukaratirwa et al., In the laboratory the partridges were 2001). It is therefore, essential to scrutinize examined internally for presence of parasites these parasites more closely to minimize the after slaying them. The feathers removed for devastating effect they have on the indigenous better approaching to abdominal organs and birds, other birds and humans. Identifying the each organ (intestine, liver, gallbladder, lung differences in climate, agro-climatic and and trachea) was transferred to Petri dishes geographic condition of the various regions is containing tap water and examined under a one way of closer scrutiny (Dube et al, 2010; dissecting microscope at 40x magnification. Magwisha et al., 2002; Saif, 2008). The gastrointestinal tract was removed out from the esophagus to the rectum and opened In general, information about the geographical longitudinally and examined carefully distribution of parasitic diseases and (Avcioglu et al., 2008). The alimentary canals localization, prevalence and intensity of were opened longitudinally. The intestine was infection, and information on the life-cycle opened, and the mucosa was scraped and (where available) in such as washed under running tap water in a 100- Tetraogallus caspius is still very limited mesh sieve, in order to recover the smaller (Akhumyan and Khanbegyan, 1982). helminths. The content was examined under a Therefore, the study of Caspian snowcock stereomicroscope and all the parasites were parasite is necessary and important to reduce collected. The collected helminths were the impact on this national wealth, to increase preserved in 70% ethyl alcohol. For the productivity, the possibility of breeding and identification purposes, nematodes were acclimatization of this bird in new locations, mounted in drops of lacto-phenol, where as and it plays an important role in spreading cestodes were stained by carmine, and both diseases and parasites to domesticated birds were later examined under the light and even to humans. microscope. The helminths were identified by using the characteristics described according The present study was undertaken to evaluate to Soulsby (1982). Identification, prevalence and intensity of the gastrointestinal helminths in Caspian Results snowcock in the different regions of the North Khorasan, Northeast of Iran. In examining the 180 alimentary tracts of the same number of partridge, it was found that Material and methods 136 partridges (i.e. 75.5%) were infected with parasitic helminths. 132 were infected with the A total of 180 Caspian stopcock (Tetraogallus cestode (73.3%) and 4 were infected by the caspius) partridges were randomly collected nematode (2.2%) singly. The number of

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partridges infected with both cestodes, and and appears to be the most intense where the nematodes were two. These findings are prolong contact occurs between the host and summarized in table 1. parasite (Atkinson et al., 2008).

Table 1. The Prevalence of helminths infection rates in The most prevalent cestodes species identified 180 partridge Caspian stopcock from the North Khorana in the present study were Anonchotaenia province, north east of Iran globata (73.3%) followed by Raillietina Number of tetragona (72.2%). The occurrence of A. Infection Parasite species partridge globata is the first record of their presence in rate (%) infected partridges from Iran; although, this cestode has Trichostrongylus 1 0.5% been reported in warbler (Alaudidae) and tenuis other birds from different Heterakis dispar 1 0.5% Anonchotaenia (Eslami et al., 2010). 132 73.3% globata Raillietina tetragona 130 72.2% With regard to the species of tapeworms found Ascaridia galli 2 1.1% R tetragona, according to Soulsby (1982) are considered to be harmful to birds. The prevalence of R. tetragona is similar to those The species and prevalence of parasitic reported by Shlemon and Saeed (2012) in helminths were as follows: the cestoda species Chukar Partridge and in chickens (Dube et al., Anonchotaenia globata and Raillietina 2010; Eslami et al., 2010; Ebrahimi et al., 2014; tetragona were the most abundant and Nayebzadeh et al., 2014). Some investigators occured at 73.3%. Of the established species of suggest that a high prevalence of Raillietina Nematoda, Ascarida galli occurred at 1.1%, spp. is related to the close-contact between the Heterakis dispar and Trichostrongylus tenuis, birds and the soil for prolonged period, were low and occured at 0.5%, which is the because the soil is suitable environment for least percentage of all. No trematodes were intermediate hosts (Ashenafi and Eshetu, 2004; found. Nayebzadeh et al., 2014).

Discussion The findings of three species of nematodes (T. tenuis, A. galli and H. dispar) represent new The aim of the present study was to find the records in Caspian snowcock (T. caspius). In prevalence of helminths in Tetraogallus caspius the present study, the prevalence of H. dispar, partridge. To our knowledge, there is no T. tenuis was 0.5% and A. galli was 1.1%. reported study on the helminths in Tetraogallus caspius partridge. Examination of The prevalence of A. galli agrees with the the Caspian snowcock partridge for helminths finding of the several studies conducted on revealed its infection with cestodes and different partridge species (Avcioglu et al., nematodes, but not with any trematode or 2008; Madsen, 1941; Rizzoli et al., 1999; acanthocephalan species. Shlemon and Saeed, 2012; Tibbitts and Babero, 1970). A. galli endangers the bird by Most worms in our investigation were consuming its food, thus causing the bird to cestodes. Cestodes are extremely common face depression, slow growth, low appetite, parasite of birds (Atkinson et al., 2008), reduced production that might be reasons might be the geographical variations in indicative of its intestinal mucosa being the distribution of the parasites or the damaged (Permin et al., 2006). intermediate hosts of the worms. (Ebrahimi et al., 2014). Adult cestodes may cause damage to The prevalence of H. dispar in this study was the gizzard lining (Gastrotaenia), intestinal low that agrees with the finding of the other blockage, localized damage to the intestinal several studies conducted on different species wall at the site of attachment, or irritation of partridge and other birds (Gonzalez et al., the intestinal lining. Inflammation is the most 2005; Park and Shin, 2010). Moreover, the common host response to cestode infection prevalence of T. tenuis infection was similar to

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that reported by Millan et al. (2004) and Purdy BirdLife I. 2012. Tetraogallus altaicus. IUCN Red List et al. (2012) and intensity of infection was low. of Threatened Species. International Union for T. tenuis can be implicated in outbreaks of Conservation of Nature. severe enteritis in birds. Moderate to severe Dube S., Zindi P., Mbanga J., Dube C. 2010. A study of infections cause diarrhea, which is often fatal. scavenging poultry gastrointestinal and endo- parasites in rural areas of Matabeleland Lighter infections result in a chronic syndrome Province, Zimbabwe. Int. J. Poult. Sci. 9(9):911- characterized by anemia and emaciation 915. (Taylor et al., 2007). Ebrahimi M., Asadpour M., Khodaverdi M., Borji H. 2014. Prevalence and distribution of The researchers recommend carrying out gastrointestinal helminths in free range periodic investigations on helminths of the chickens in Mashhad, northeast of Iran. Sci. Caspian snowcock, as well as any other Iran Parasitol. 15:38-42. wild species wherever possible. This study Eslami A., Ghaemi P., Meshgi B., Bhadry Sh.R. 2010. sheds new light on the severity of the Study helminth infection of warbler (Alaudidae) prevalence of gastrointestinal helminths in golestan. Large Anim. Clinic Res. (Veterinary) 4(12):27-30. infections of indigenous Caspian stopcock of Gonzalez D., Skewes O., Candia C., Palma R., Moreno North Khorasan region that has its own agro- L. 2005. Estudio del parasitismo climatic characteristics, and the country of Iran gastrointestinal y externo en Caiquén has highly diverse geographic and agro- Chloephaga picta Gmelin, 1789 (Aves, Anatidae) climatic conditions. On the other hand this en la región de Magallanes, Chile. Parasitol. study could be useful to evaluate the wildlife Latinoam. 60:86-89. situation and the dangers of dissemination of Madsen H. 1941. The occurrence of Helminths and some of the parasitic species to the Coccidia in Partridges and Pheasants in economically important , pets and Denmark. J. Parasitol. 27:29-34. humans. Magwisha H.B., Kassuku A.A., Kyvsgaard N.C., Permin A. 2002. A Comparison of the Prevalence and Burdens of Helminthic Acknowledgments Infections in Growers and Adult Free-range Chickens. Trop. Anim. Health Prod. 34:205-214. We thank Dr. S.H. Hosseini professor of Millan J., Gortazar C., Villafuerte R. 2004. Ecology of Veterinary Parasitology, School of Veterinary nematode parasitism in red-legged partridges Medicine, Tehran University, Iran, Dr. Sina ( rufa) in Spain. Helminthologia Faghihzadeh, Dr. Z. asadoallhi and Dr. M. 41(1):33-34. Ebrahimi for his kind assistance. The authors Mukaratirwa S., Hove T., Esmann J.B., Hoj C.J., declare that they have no conflict of interest. Permin A., Nansen P. 2001. A survey of parasitic nematode infections of chickens in rural Zimbabwe. Onderstepoort J. Vet. 68(3):183-186. Mwale M., Masika PK. 2011. Point prevalence References study of gastro-intestinal parasites in village chickens of Centane district, South Africa. Afr. Akhumyan K.S., Khanbegyan R.A. 1982. The J. Agric. Res. 6:2033-2038. helminth fauna of wild Galliformes in Armenia Nayebzadeh H., Ahmadi A., Ebrahimi M. 2014. ( coturnix, Alectoris graeca, Perdix Gastrointestinal Helminthic Infections of Local perdix, Lyrulus mlokosiewiczi and Tetraogallus Chickens, Kept under the Traditional System in caspius). Zoologicheskii Sbornik, Akademiya the Isfahan Region, Center of Iran. J. Fac. Vet. Nauk Armyanskoi SSR, Institut Zoologii 18:9-45. Med. Istanbul Univ 40(2):237-242. Ashenafi H., Eshetu Y. 2004. Study on Park S., Shin S.S. 2010. Concurrent Capillaria and gastrointestinal helminths of local chickens in Heterakis Infections in Zoo Rock Partridges, Central Ethiopia. Rev. Méd. Vét. 155(10):504- Alectoris graeca. Korean J. Parasitol. 3:253-257. 507. Permin A., Christensen J.P., Bisgaard M. 2006. Atkinson T., Thomas N.J., Bruce H.D. 2008. Parasitic Consequences of concurrent Ascardia galli and Diseases of Wild Birds. Blackwell, 592 pp. Escherichia coli infections in chickens. Acta Vet. Avcioglu H., Burgu A., Bölükbas C.S. 2008. Ascaridia Scand. 47(1):43-54. numidae (Leiper, 1908; Travassos, 1913) in Purdy D., Aebischer N.J., Davis C. 2012. Comparison Rock Partridge (Alectoris chukar) in Turkey. of single and split-dose flubendazole treatment Parasitol. Res. 102:527-530. for the nematode parasite Trichostrongylus tenuis in experimentally infected grey

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